taxonomic re-assessment of kindbergia (brachytheciaceae ......the brachytheciaceae are a moss family...

Cryptogamie, Bryologie, 2015, 36 (1): 47-68© 2015 Adac. Tous droits réservés

doi/10.7872/cryb.v36.iss1.2015.47

Taxonomic re-assessment of Kindbergia (Brachytheciaceae, Bryophyta) in China, with a

description of Pseudokindbergia gen. nov.

Min LIa,b, Jing MAa, Michael S. IGNATOVc, Benito C. TANd,Sanna HUTTUNENe, Jian-Cheng ZHAOb & You-Fang WANGa*

a School of Life Sciences, East China Normal University, Shanghai, China

b College of Life Science, Hebei Normal University, Shijiazhuang, China

c Tsitsin Main Botanical Garden of Russian Academy of Sciences, Moscow, Russia

d The University and Jepson Herbarium, University of California at Berkley, California, USA

e Department of Biology, University of Turku, Finland

Abstract −−−− The distribution and systematic position of Kindbergia Ochyra in China is re-evaluated. The phylogenetic analyses based on nuclear marker (ITS1-5.8S-ITS2) andchloroplastic markers (rpl16, trnG, and trnL-F) show that the alleged species of“Kindbergia” in China and Himalayas form a maximally supported clade (1.00 PP and 100MPBS), which is closely related to the clade of Brachythecium Schimp., EurhynchiadelphusIgnatov et Huttunen, and Myuroclada Besch., whereas the other Kindbergia specimens fromAfrica, America, Europe, Japan and the Southern Hemisphere form a monophyletic group,which is sister to Scleropodium Schimp. The specimens of Chinese species of “Kindbergia”are found, both molecularly and morphologically, to be identical with the HimalayanK. dumosa (Mitt.) Ignatov et Huttunen, and differ from Kindbergia specimens from otherregions in the world in the shape of proximal branch leaves, operculum shape and capsuleorientation. A new monotypic genus Pseudokindbergia M. Li, Y.F. Wang, Ignatov etB.C. Tan, is established to accommodate only the generitype P. dumosa (Mitt.) M. Li,Y.F. Wang, Ignatov et B.C. Tan, comb. nov. (≡ Hypnum dumosum Mitt.), and Bryhniaserricuspis (Mitt.) Y.F. Wang et R.L. Hu (≡ Eurhynchium serricuspis Mitt.) is consideredsynonymous with it.

Molecular phylogeny / Brachytheciaceae / Kindbergia / Pseudokindbergia / China

INTRODUCTION

The Brachytheciaceae are a moss family wthin which over 50 generawere recognized, and for a long time they were a point of taxonomic disagreementamong different authors. Having an extremely variable morphology and lackingoften distinctive taxonomic characters, even in various combination, that are

* Corresponding author: [email protected]

48 M. Li et al.

specific for one genus, the family has earned the reputation as one of the mosttaxonomically difficult groups among mosses. The species referred to the genusKindbergia in the middle of 20th century were often placed in EurhynchiumSchimp. and frequently confused with species of Oxyrrhynchium (Schimp.)Warnst., until the conservation of the latter with the conserved type wasintroduced (Ignatov & Isoviita, 2003). This action was deemed necessary asK. praelonga (Hedw.) Ochyra, the type of the genus Kindbergia, had beenconsidered by some authors as the type of the genus Oxyrrhynchium. The longhistory of the misapplication of the species name “praelongum” was described indetails by Touw & Knol (1978). Noteworthy to mention that in all the currentclassification systems of the family based on molecular phylogenetic studies(Ignatov & Huttunen, 2002; Vanderpoorten et al., 2005; Huttunen et al., 2007), thethree genera, Kindbergia, Eurhynchium and Oxyrrhynchium, belong to threedifferent subfamilies.

The genus Kindbergia Ochyra was originally segregated by Robinson(1967) as Stokesiella (Kindb.) Robins. Since the name appeared to be anillegitimate later homonym of Stokesiella Lemmerm. of 1908, Ochyra (1982)proposed a new replacing name, Kindbergia. Many bryologists had followed thesuggestion (Giles, 1990; McFarland, 1994; Crosby et al., 1999; Ignatov &Huttunen, 2002; Huttunen & Ignatov, 2004; Huttunen et al., 2007; Goffinet& Shaw, 2008; Frey & Stech, 2009). However, the genus was not accepted byKoponen (1987), Buck (1988), Noguchi et al. (1991), and Iwatsuki (2004).

In China, the species distribution of the genus Kindbergia is not clear andrather controversial. Brotherus (1929) reported K. praelonga [as Eurhynchiumstokesii (Turner) Schimp.] from Hunan Province, which later was proven to be aphenotypic expression of Bryhnia novae-angliae (Sull. et Lesq.) Grout with longerleaf apex (Ignatov et al., 2005). Several authors reported K. praelonga in Chinasuccessively (Bai, 1997; Zhao & Cao, 1998; Hu & Wang, 2000). Oxyrrhynchiumbiforme Broth. and Bryhnia serricuspis (Müll Hal.) Y.F.Wang et R.L.Hu, bothendemic to China, were synonymized with K. praelonga by Koponen (1987) andIgnatov et al. (2005). Redfearn et al. (1996) included two species and one varietyin the genus Kindbergia in China, namely K. arbuscula (Broth.) Ochyra,K. praelonga, and K. praelonga var. stokesii (Turner) Ochyra. However, Hu &Wang (2005) and Hu et al. (2008) accepted only one species, K. arbuscula, for theChinese moss flora, and put it in the genus Eurhynchium.

Recent molecular phylogenetic data provide a lot of evidences forsegregation of additional small genera in the family (Huttunen & Ignatov, 2004;Ignatov et al., 2008; Aigoin et al., 2009a, b; Ignatov et al., 2010). The status ofKindbergia as a separate and well-defined genus was confirmed by all the recentstudies (Huttunen & Ignatov, 2004; Vanderpoorten et al., 2005, etc.).Notwithstanding, an expanded analysis of the genus was undertaken by Hedenäs(2010) based on the nuclear ITS and chloroplastic tRNA-Gly. His sampling oftaxa covered the range of the genus woldwide, showing the very wide distributionof Kindbergia praelonga in Europe and Macaronesia, SW Asia, Africa, Australiaand New Zealand. The North and South American plants of K. praelonga thatwere morphologically virtually indistinguishable from European plants werefound to be somewhat different in their genetic constitution. On the other hand,the morphologically distinct K. arbuscula from Japan did not exhibit anydifferences in the sequence of chloroplastic DNA studied (nuclear marker was notstudied). Therefore Hedenäs (2010) suggested that South American plants andmost of North American ones are likely to represent another species, whichhowever still awaiting a thorough revision. At the same time, specimens of

Taxonomic re-assessment of Kindbergia in China 49

Chinese K. praelonga (including Bryhnia serricuspis) appeared to be even moredifferent in their DNA sequence alignment from the European and Americancounterparts. Hedenäs (2010) concluded that the Chinese and Himalayanpopulations of Kindbergia may be conspecific and suggested that K. dumosa(Mitt.) Ignatov et Huttunen, a moss described from the eastern Himalayas(Gangulee, 1978; Vohra, 1983), be used as the proper name of the combinedtaxon. However, only four sequences of three Chinesse samples were involved inthe study of Hedenäs (2010), while the Himalayan material of K. dumosa was notobtained for the study as the species is not common in distribution. Thus, thenecessity of another expanded analysis of the East Asian materials of Kindbergiaremains and this problem is specifically addressed in the present study.

MATERIALS AND METHODS

Morphological investigation

Except for Kindbergia kenyae (Dixon ex Tosco et Piovano) O’shea etOchyra, a total of 295 collections of other seven Kindbergia species, namelyK. africana (Herzog) Ochyra, K. arbuscula, K. oedogonium (Müll.Hal.) Ochyra,K. oregana (Sull.) Ochyra, K. praelonga, K. squarrifolia (Broth. ex Iishiba)Ignatov et Huttunen, and K. dumosa were studied. All these specimens wereloaned from BM, DUKE, FH, FI, HIRO, HSNU, JE, KUN, MHA, MO, NY, PE,S, SHNU, SZG, and TNS. A number of characters, such as growth form, leafshape and dimensions, lamina cell length, shape of proximal branch leaves, shapeof operculum, and capsule orientation etc., were investigated. Sporophytes are notcommon in Chinese plant materials, and only nine samples with capsules werestudied. Fortunately, European and American collections with sporophytes wererelatively numerous, allowing a reliable observation and evaluation.

Molecular taxon sampling

Seventy-eight samples belonging to the representative genera of thethree subfamilies across the family Brachytheciaceae were used for the molecularanalyses (see Appendix). Except for Brachytheciella Ignatov, which is known onlyby the holotype in H and is morphologically quite divergent from Kindbergia, allgenera of the subfamily Brachythecioideae Engler (incuding HomalothecioideaeIgnatov et Huttunen) were included as the in-groups: Brachytheciastrum Ignatovet Huttunen, Brachythecium (including Bryhnia Kaurin), EurhynchiadelphusIgnatov, Huttunen et T.J. Kop., Eurhynchiastrum Ignatov et Huttunen, FrahmiellaIgnatov, Vanderpoorten et Wang You-fang, Homalothecium Schimp., Kindbergia,Myuroclada Besch., Sciuro-hypnum (Hampe) Hampe, Scleropodium, andUnclejackia Ignatov, T.J.Kop. et D.H.Norris (see also Ignatov & Huttunen, 2002;Vanderpoorten et al., 2005; Frey & Stech, 2009; Li et al., 2014). Within the genusKindbergia, four of eight species were sampled: K. arbuscula, K. dumosa,K. oregana (Sull.) Ochyra, and the type species, K. praelonga. These are thespecies studied also by Hedenäs (2010). The remaining four species of the genuscould not be included in our study because of no available recent collections.

50 M. Li et al.

In our study we sampled twenty specimens of alleged taxa of the genusfrom China representing different climatic regions of the country and alsomaximally the differentiated morphotypes. Four specimens of K. dumosa fromIndia and Bhutan collected from different altitudinal belts in the Himalayas weresequenced as well. Outgroups include representative members of the other twosubfamilies of Brachytheciaceae, Eurhynchioideae Milde (Rhynchostegium) andHelicodontioideae M.Fleisch. (Cirriphyllum and Oxyrrhynchium) (Frey & Stech,2009). The resulting tree of the family is rooted on one of two analyzedrepresentatives of Meteoriaceae, a sister family to Brachytheciaceae (Huttunen &Ignatov, 2004).

Molecular protocols

DNA extraction followed the protocols described by Sun et al. (2000).One nuclear and three plastid markers were chosen: nuclear ribosomal internaltranscribed spacer region ITS1-5.8S-ITS2 (hereafter, ITS), ribosomal protein L16(hereafter, rpl16), tRNA (Gly) (UCC) (hereafter, trnG) and trnL-trnF intergenicspacer (hereafter, trnL-F). These four regions have been widely used inphylogenetic analyses of pleurocarpous mosses (eg. Huttunen & Ignatov, 2004;Huttunen et al., 2007; Draper & Hedenäs, 2009; Hedenäs, 2010, 2011a, b, 2012;Li et al., 2014). The following primers were used to amplify the different markers:“18SF” and “26SR” for the ITS region, or sometimes, “18SF” and “5.8SR” forITS1, and “5.8SF” and “26SR” for ITS2 (Hartmann et al., 2006); “F71” (Jordan etal., 1996) and “antR2” (Hedenäs & Eldenäs, 2007) for rpl16; “trnGF” and“trnGR” for trnG (Pacak & Szweykowska-Kulinska, 2000); and “trnC” and “trnF”for trnL-trnF region (Taberlet et al., 1991). For ITS and trnL-F, the PCR cyclesused an initial denaturation step of 3 minutes at 95°C, followed by 35 cycles of30 seconds at 95°C, 30 seconds at 50°C, 90 seconds at 72°C, and a final elongationof 5 minutes at 72°C. For trnG and rpl16, it began with an initial denaturationstep of 5 minutes at 80°C, followed by 34 cycles of 1 minute at 95°C, 1 minute at50°C (58°C for rpl16), 4 minutes at 65°C, and a final elongation of 5 minutes at65°C. PCR products were purified with the Gel Extraction Kit (Cwbio, Shanghai,China) following the manufacturer’s protocol. These purified PCR products weresequenced by Life Technologies Inc., China (www.lifetechnologies.com).

Sequence editing, alignment and phylogenetic analyses

Sequence chromatograms were compiled using SeqMan II (DNASTARInc., Madison, WI, USA) and then aligned manually in PhyDE 0.9971 (Müller et al.,2010). Regions of partially incomplete data at the beginning and end of thesequences were identified and excluded from subsequent analyses. Using simpleindel coding as proposed by Simmons & Ochoterena (2000), indels were codedwith SeqState (Müller, 2005). Both Maximum parsimony (MP) and Bayesianphylogenetic analyses were conducted as both of them were used by previousauthors analyzed this group. For the MP analysis, command files for the parsimonyratchet (Nixon, 1999) were generated using the program PRAP2 (Wall et al., 2008)and executed with the program PAUP 4.0b10 (Swofford, 2003) using TBR branchswapping with character states specified as unordered and unweighted. Bootstrapanalysis was performed with 10000 replicates and random taxon addition with100 replicates. For the Bayesian analysis, after optimal nucleotide substitutionmodels for each region were calculated using MrModeltest v.2.3 (Nylander, 2004)


in PAUP 4.0b10 (Swofford, 2003), the relevant parameters were set accordinglyto corresponding values independently derived from each model. Phylogeneticanalyses were then conducted under a Bayesian Markov Chain Monte Carloapproach using MrBayes v.3.2.1 (Huelsenbeck et al., 2001). Four parallel runs,each with four chains, were run for 5000000 generations, with trees being sampledevery 1000 generations.

Phylogenetic trees were constructed for the individual loci in eachanalysis. As some samples studied for phylogenetic analyses have only thesequences of ITS or part of the four markers, the chloroplastic dataset include 59of the 78 samples respresenting most of the genera in Brachythecioideae.Topological conflicts were considered significant if two different relationships forthe same set of taxa were both supported by Bayesian posterior probability (PP)(> 0.95) and with bootstrap support values from the MP (MPBS) (> 75). Whenthere was no conflict between the nuclear and chloroplast partitions, thephylogenetic analyses were reconstructed based on combined dataset of ITS,rpl16, trnG, and trnL-F regions. TreeGraph 2 (Stöver & Müller, 2010) was usedto summarize the topology and support from maximum parsimony and Bayesiananalyses.

RESULTS

Evaluation of distinguishing morphological characters

Our preliminary evaluation made for a number of characters such asgrowth form, leaf shape and dimensions, and lamina cell length etc., yieldedstrong overlapping observation among all seven Kindbergia species (not shown).While Chinese Kindbergia species and K. dumosa from Himalayas are clearlydifferent from extra-Chinese and other species in the shape of proximal branchleaves (previously often called pseudoparaphyllia, but see discussion of Spirina et al.(2012) and Ignatov & Spirina (2012)), the shape of operculum, and capsuleorientation (Table 1; Figs 1-21).The Chinese + Himalayan species of Kindbergiahave semi-orbicular to orbicular-triangular, obtuse or truncate proximal branchleaves, conic-apiculate operculum, and an inclined capsule, whereas those of thespecies of the genus from the rest of the world are ovate-apiculate, ovate-acuminate to triangular proximal branch leaves, long-rostrate operculum, and ansubpendent to horizontal capsule.

In addition, the differences shown in the shape of proximal branchleaves, the shape of operculum, and capsule orientation, were found to be ratherreliable and congruent among and within the molecularly delimited plant groups(Table 1; Figs 1-24). In all cases, the shape of proximal leaves of a shoot is easyto study and has taxonomic value.

Phylogenetic reconstruction

Except for the clade of Sciuro-hypnum and BME clade which areresolved differently in the nuclear and chloroplastic topologies, the well supportedmajor clades resolved by both dataset were the same, and the combined tree was

52 M. Li et al.

better resolved than any of the separate trees and the support values weresubstantially increased as well (Figs 22-24). Thus we used the combined datasetfor further analyses.

After the deletion of incomplete regions of the gene sequences at thebeginning and end of the alignment for some specimens, the total number ofaligned sites of the four loci and coded indels used in the present study contains2669 bp pairs. Among them, 872 positions belong to the nuclear compartment,1588 positions for the plastid genes, and 209 for coded indels. The number of sites

Table 1. A morphological comparison among species of Kindbergia

Taxon Proximal branch leaves OperculumCapsule

orientationDistribution

K. africana triangular-acuminate not seen not seen Uganda,South Africa

K. arbuscula ovate-apiculate long-rostrate subpendent Japan

K. dumosa semi-orbicular, truncate conic-apiculate inclined India, Bhutan, Nepal

K. dumosa (“K. arbuscula”)

semi-orbicular, truncate conic-apiculate inclined China

K. dumosa (Bryhnia serricuspis)

triangular, obtuse not seen not seen China

K. oedogonium ovate-acuminate long-rostrate horizontal Bolivia

K. oregana ovate-acuminate long-rostrate subpendent Canada, USA

K. praelonga ovate-acuminate to triangular-acuminate

long-rostrate subpendent Africa, Australia, Europe,America, West Asia

K. squarrifolia triangular-acuminate not seen not seen Japan

Table 2. Numbers of sites in each locus and coded indels based on sequence length (bp), variable (v.) sites, informative (i.) sites, and the models selected for Bayesian analysis

Gene Length (bp) v. sites i. sites Model

Nuclear compartment ITS 872 238 151 GTR+I+G

Plastid compartment rpl16 707 131 82 GTR+I+G

trnG 523 76 46 GTR+I

trnL-F 358 40 18 HKY+I+G

Coded indels 209 215 123 variable

Total 2669 700 420 ---------


in each locus and coded indels based on sequence length, variable sites, parsimonyinformative sites and the optimal substitution models selected for Bayesiananalysis are given in Table 2.

The topologies are mostly identical after a comparison between the MPanalysis (number of the most parsimonious trees = 1, length= 1240 steps;Consistency Index = 0.633; Retention Index = 0.842) and the Bayesian analysis(-lnL = 10199.152) (trees not shown). Thus, only the Bayesian consensus tree forthe combined dataset is here presented as the main data outline (Fig. 24). TheBayesian posterior probabilities (PP), as well as the bootstrap support values fromMP analysis (MPBS), are labeled on the branches respectively.

Figs 1-11. The shape of proximal branch leaves in the genus Kindbergia1. K. praelonga (Canada, W.B. Schofield 12822, MO 5147535). 2. K. praelonga (Australia,H. Streimann 42657, SB96040). 3. K. praelonga (Portugal, Fontinha 2, SB22292). 4. K. squarrifolia(isotype: Japan, H. Sasaoka 13678, TNS 174038). 5. K. oregana (isotype: Oregon, NY 00734140).6. K. oedogonium (possible type: Germain s.n., NY 01274075). 7. K. arbuscula (Japan,E. Nokubo 31, HIRO). 8. K. africana (isotype: L. Haumann 69, SB82905). 9. K. dumosa(lectotype: India, J.D. Hooker 1041, NY 01179094). 10. K. dumosa (“K. arbuscula”) (China,M.Z. Wang 6477, PE). 11. K. dumosa (Bryhnia serricuspis) (isotype: China, J. Giraldi s.n., FI).

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Figs 12-21. Capsule orientation and the shape of operculum in the genus Kindbergia12-13. K. dumosa (“K. arbuscula”) (China, M.Z. Wang 6477, PE); 14-15. K. dumosa (lectotype:India, J.D. Hooker 1041, NY01179094); 16. K. arbuscula (holotype: Japan, JE ); 17-18. K. praelonga(Canada, W.B. Schofield 12822, MO 5147535); 19. K. oregana (isotype: Oregon, NY 00734140);20-21. K. oedogonium (possible type: Germain s.n., NY 01274075).

Fig. 22. Fifty percent majority-rule consensus tree from Bayesian analysis of dataset of 78 samplesbased on ITS. Bayesian posterior probabilities (>0.95) (above) and MP boot-strap support values(>75) (below) are shown on the branches respectively.

▲

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Fig. 23. Fifty percent majority-rule consensus tree from Bayesian analysis of the combineddataset of 59 samples based on rpl16, trnG, and trnL-F. Bayesian posterior probabilities (>0.95)(above) and MP boot-strap support values (>75) (below) are shown on the branches respectively.


Fig. 24. Fifty percent majority-rule consensus tree from Bayesian analysis of the combineddataset of 78 samples based on ITS, rpl16, trnG, and trnL-F. Bayesian posterior probabilities(>0.95) (above) and MP boot-strap support values (>75) (below) are shown on the branchesrespectively.

58 M. Li et al.

All Chinese “Kindbergia” samples, including those identified previouslyas K. arbuscula, K. praelonga and Bryhnia serricuspis, as well as K. dumosa fromthe Himalayan region, were resolved monophyletically (hereafter, as KindbergiaII clade) with a maximal support of 100% (Fig. 24). It forms a sister clade to theBrachythecium-Myuroclada-Eurhynchiadelphus clade (hereafter designated asBME clade). The two samples of Sciuro-hypnum were resolved as a monophyleticclade as well (1.00 PP and 100 MPBS) and formed the sister clade of theKindbergia II clade, plus the BME clade. No geographic segregation wasdemonstrated within the Kindbergia II clade, and recongnition of morphotypesrelated to the above mentioned names was not supported by any of the performedanalyses. Kindbergia praelonga from Africa, America, Australia and Europe,K. oregana from America and K. arbuscula from Japan formed a robust clade(hereafter designated as Kindbergia I clade) (1.00 PP and 99 MPBS), which isdistantly separated from Kindbergia II clade by members of Homalothecioideae,Frahmiella, Eurhynchiastrum, Homalothecium and Brachytheciastrum. TwoScleropodium samples form a maximally supported clade (1.00 PP and 100 MPBS)which is sister to the rest of Brachythecioideae, including genera Kindbergia,Frahmiella, Eurhynchiastrum, Homalothecium, Brachytheciastrum, Sciuro-hypnum, Brachythecium, Myuroclada, Eurhynchiadelphus, and Kindbergia IIclade.

Within the genus, K. oregana, K. arbuscula, and K. praelonga were shownto be monophyletic speices (1.00 PP and 73 to 100 MPBS). No subclades withinKindbegia I clade got any support. The two sublades of Kindbegia I clade have apoor correspondence to the geography of their range. Although all fourHimalayan specimens were placed together in one of the two subclades, includingsamples from Taiwan, Yunnan, Hunan and Shaanxi, and yet, another subcladeincluded also specimens from Taiwan, Yunnan, and Gansu, in addition to samplesfrom Sichuan, Hunan, Shaanxi.

DISCUSSION

The general tree topology

Our newly obtained results of the phylogenetic analyses are very similarto what has been found previously by Aigoin et al. (2009a), Huttunen & Ignatov(2004), Ignatov et al. (2008), and Vanderpoorten et al. (2005). TheEurhynchioideae (Rhynchostegium) occupies a basal position on the tree. Thenext in the grade is Helicodontioideae, and the terminal clade includedrepresentatives of Brachythecioideae s.l. Although species referred originally toHomalothecioideae shows in some analyses a segregation of Homalothecium plusBrachytheciastrum and sometimes also Frahmiella plus Eurhynchiastrum, thesupporting value was low, and the uncertain position of Kindbergia, Sciuro-hypnum and Scleropodium are obviously in favor of treating Brachythecioideae ina broad sense, as suggested by Vanderpoorten et al. (2005).

It is interesting to make a comparison of the topology of the phylogenetictrees of Brachytheciaceae generated by our study and that published in Hedenäs(2010). Representatives of Chinese Kindbergia were found in both studies to bethe most isolated group positioned quite distantly from the taxa of K. oregana,


American K. praelonga, and European+West Asiatic+Africa+AustralianK. praelonga. However, in contrast to the report of Hedenäs (2010), the positionof Japanese K. arbuscula was shown in our study to be more isolated fromK. praelonga than from K. oregana. This difference in topology, obviously, isbrought by the lacking of ITS data in the dataset of Hedenäs (2010). In our study,

Figs 25-41. Pseudokindbergia dumosa (Mitt.) M.Li, Y.F.Wang, Ignatov et B.C.Tan 25-26. Stem leaves; 27-28. Branch leaves; 29. Cells at apex of stem leaf; 30. Leaf border in themiddle of stem leaf; 31-32. Median laminal cells of stem leaf; 33. Leaf base; 34. Leaf decurrency ofthe stem leaf; 35. Basal cells near leaf decurrency; 36. Basal cells near costa; 37. End of the costain stem leaf (arrow pointing at spines on leaf costa); 38. Cross section of stem; 39. Innerperichaetial leaf; 40. Capsule; 41. Surface of the seta (from lectotype of Kindbergia dumosa:India, J.D. Hooker 1041. NY 01179094).

60 M. Li et al.

the core genera of Brachythecioideae, namely Brachythecium, Sciuro-hypnum,Myuroclada, Eurhynchiadelphus form a moderately supported clade whichincludes also Chinese and Himalayan Kindbergia II clade (Fig. 24). Each of therest of the genera, namely Kindbergia (clade I), Eurhynchiastrum, Frahmiella,Scleropodium, Homalothecium and Brachytheciastrum were shown to bemonophyletic. Moderate support was shown for the clade of Brachytheciastrum+Homalothecium (1.00 PP and 73 MPBS) and maximal support for Frahmiella andEurhynchiastrum (1.00 PP and 100 MPBS). Shown in a previous analysis reportedby Ignatov et al. (2010), the clade of Frahmiella and Eurhynchiastrum received apoor support in a MP phylogram.

The inclusion in analysis of all the genera of Brachythecioideae (exceptfor the obviously unrelated Brachytheciella) and Homalothecioideae brought outanother unexpected result. It shows clearly the presence of a topological gapbetween the Chinese+Himalayan species of “Kindbergia” and the populations ofthe species of this genus from the rest of the world. To witness, this topologicalgap is filled by a clade that included taxa belonging to the core ofBrachythecioideae (see Fig. 24). Furthermore, the set of characters of somewhatdendroid plant habit, dimorphic leaves, strong and nearly percurrent costa anddistinctive leaf base decurrency can separate the Chinese+Himalayan of“Kinbergia” (Kindbegia II clade) from other species of related genera, such asBrachythecium, Eurhynchiadelphus and Myuroclada. Thus, the genus Kindbergiain its current circumscription appears to be polyphyletic, suggesting a neededsegregation of the Chinese and Himalayan representatives of Kindbergia II cladeas a separate genus.

Fig. 42. Schematic map of the world distribution of Kindbergia (solid circles) andPseudokindbergia (open circles). Mapping is designed mainly on the country, or in biggercountries, at state/province level, using databases of NY, MO, S, Flora of North America (seeIgnatov, 2014), China (Hu et al., 2008), publications on the distribution in Africa (O’Shea, 2006),Europe (Duell, 1984, 1985), West Europe and North Asia (Ignatov et al., 2006), MediterraneanRegion (Ros et al., 2013), Middle East (Kürschner & Frey, 2011) and Australia (Hedenäs, 2002),and treatment of genus Kindbergia (Hedenäs, 2010.)


Pseudokindbergia M. Li, Y.F. Wang, Ignatov et B.C. Tan, gen. nov.

Diagnosis: The new monotypic genus is close in morphology to KindbergiaOchyra, but differs in having semi-orbicular to orbicular-triangular, obtuse ortruncate proximal branch leaves (ovate-acuminate, ovate-apiculate to triangular-acuminate in Kindbergia), conic-apiculate operculum (long rostrate inKindbergia), and an inclined capsule (subpendent to horizontal in Kindbergia) (seeTable 1; Figs 1-21).Generitype: Pseudokindbergia dumosa (Mitt.) M. Li, Y.F. Wang, Ignatov etB.C.Tan , comb. nov. (Figs 25-41)[Basionym: Hypnum dumosum Mitt., J. Linn. Soc. Bot. Suppl. 1:80. 1859. Type:India, Sikkim, Himalaya orient. reg. temp., J.D. Hooker (No. 1041) (Lectotypeselected here: NY 01179094! Isotype: S B200108!) ≡Kindbergia dumosa (Mitt.)Ignatov et Huttunen, Arctoa 11:263. 2002]. =Eurhynchium serricuspis Müll Hal., Nuovo Giorn. Bot. Ital., n.s., 5:197.1898=Bryhnia serricuspis (Müll Hal.) Y.F. Wang et R.L. Hu, Acta Phytotax. Sin. 41:272. 2003. Type: China interior, prov. Schen-si sept., prope In-kia-po, Sept. 1896.[Lectotype (vide Koponen 1987: p.513): H-BR (non vidi); isotypes: FI! BM001030716!), syn. nov.]

Illustrations: Gangulee, 1978: Fig. 874 (p. 1138); Hu et al., 2008: Fig. 529 (p. 122);Ignatov et al., 2005: Fig. 2 (p. 11).

Species description: Plants medium-sized to robust, green to brownish-green. Stemprostrate, dendroid or subpinnately branched, with central strand or not distinct;branches straight densely or moderately densely, julaceously foliate or not.Axillary hairs 3-4-celled, 1-2 basal cells colored, to 80 µm long and 80 µm wide.Proximal branch leaves semi-orbicular to orbicular-triangular, obtuse or truncate.Stem leaves broadly triangular, 1.2-2.2 mm × 0.5-1.2 mm, tapered to lanceolateacumen, at base cordate and longly, broadly decurrent, rarely slightly so; marginserrate above, serrulate below; costa stout, nearly percurrent; median laminal cellsrhombic to rhomboidal, 20-52(-70) µm × 3-6(-8) µm, with rounded ends,moderately thick-walled, sometimes prorate; subalar cells hexagonal to shortlyrectangular, relatively large and thin-walled, 11-30(-45) µm × 8-15(-20) µm,forming indistinctly delimited group. Branch leaves smaller, triangularly ovate-lanceolate to ovate-lanceolate, 1.0-1.6 mm × 0.6-0.9 mm, acuminate, with morestrongly serrate margin. Median laminal cells 24-39(-60) µm × 3-5 µm. Dioicous.Perichaetial leaves lanceolate, ecostate, with reflexed acumen. Seta 2.0-3.0 cmlong, blackish when old, twisted, rough in surface texture. Capsule inclined.Annulus present. Operculum conic-apiculate.Specimens examined: Bhutan. Wangdue Phodrang Distr., G. & S. Miehe 00-420-18, G. &S. Miehe 98-373-9 (MHA); Lhuntse Distr., G. & S. Miehe 00-441-25 (MHA). China.Chongqing, F.X. Li 1269 (PE); Gansu Prov., F.X. Li 839, Z.T. Zhao & N.N. Yu 20061589,20061337, 20061536, 20061252 (PE); Hunan Prov., T. Koponen et al. 52381(KUN)T. Koponen et al. 52771, 52381 (MHA); Shannxi Prov., P.C. Chen et al. 632, 649 (PE),J. Giraldi s.n. (FI, BM), M. Wang 553 (KUN), Y.F. Wang et al. 374, 37 (HSNU), Z.P. Wei6476 (PE); Sichuan Prov., D.Z. Xie & J.G. Li 0059 (PE), L.Y. Pei 042, 265, 492 (PE), M.Z.Wang 49995, 50787, 50916, 51066, 57354, 58151, 58158, 58378, 58743, 58749, 860026c,860067e, 860661, 860663a, 860669, 860678, 860717, 860772, 860840 (PE), M.Z. Wang & Y. Jia510846, 51138 (PE), X.Y. Hu 0391, 0414, 0546, 0571, 0752a, 0762, 0764 (PE), P.C. Wu 22218(PE), Y. Jia J06811, J06958, J06966, J06849, J06823, J06824, J06825, J06833 (PE), Y. Liu 285,515, 524, 528, 536 (PE), Q. He 663, 930, 1095, 1107, 1146 (PE), S.Q. Sun 231 (SHNU), T. Cao& B.R. Zuo 90592, 90659, 91047 (SHNU), Y.H. Wu s.n. (HSNU), X.Y. Li & S.Q. Sun 9(HSNU); Taiwan, J.R. Shevock 17918 (MO5219552), M. Li 203 (HSNU), S. He 36270

62 M. Li et al.

(MO5355044), Y.F. Wang & M. Li 202 (HSNU); Xizang Prov., S.Y. Ge 1499 (MO3675628);Yunnan Prov., D.G. Long 35981 (KUN), M.Z. Wang 6477 (PE), Q. Liu & Q. Zuo 1290(HSNU). India. Sikkim, Sinchul, J.D. Hooker 1041 (NY 01179094, S B200108);Uttarakhand, Garhwal Himal, M. Lüth 6643 (MHA).

Distribution: Bhutan, China (Taiwan, mainland China), Nepal and India,occurring from low elevation to above 4000 m in Himalayan region.

This species is very polymorphic, which explains its confusion in earlierpublications with Kindbergia (Eurhynchium) arbuscula (Redfearn et al., 1996; Hu& Wang, 2005; Hu et al., 2008) and K. praelonga (Redfearn et al., 1996; Ignatovet al., 2005; Hu et al., 2008). It is an interesting fact that the distribution of thespecies of Pseudokindbergia does not overlap with that of Kindbergia (Fig. 42).The latter genus has a distribution in Northern Hemisphere much similar to thatsometimes called Mediterranean disjunctive of the West-West pattern (Schofield,1988; Ignatov, 1993), which includes western parts of both Eurasia and NorthAmerica. Kindbergia species occur also in western part of South America, Eastand South Africa. Likely as a result of introduction, K. praelonga occurs inAustralia and New Zealand. However, Kindbergia does not occur in India andChina, according to our present study, and this gap is filled by ecologically andmorphologically similar plants of Pseudokindbergia.

Do Kindbergia arbuscula and K. praelonga occur in China?

Pseudokindbergia dumosa is characterized by a strong branching habit,looking very much like Kindbergia arbuscula, another species with also a strongbranching habit. The molecular data, however, showed that this character ishomoplasious. The very similar subdendroid plants of ‘K. arbuscula’ fromSW China were shown in the molecular phylogenetic tree to be located within thePseudokindbergia clade (see Fig. 24). Similarly, the weakly branching specimensof P. dumosa collected from various parts of China, almost indistinguishable fromsome phenotypes of European K. praelonga, were proven by the DNA sequenceanalysis to be plants of Pseudokindbergia. This conclusion is confirmed further byour study of the proximal branch leaves of the Chinese specimens which alwaysshown to be of the Pseudokindbergia type (semi-orbicular to orbicular-triangular,obtuse or truncate), and not the Kindbergia type (ovate-acuminate, ovate-apiculate to triangular-acuminate) (Table 1; Figs 1-11).

Based on our study, we conclude that K. arbuscula represents a distinctspecies endemic to Japan. This Japanese endemic is shown by our study to bemore distantly related to K. praelonga than what was stated in Hedenäs (2010).The signal from the ITS gene sequences indicates that the former species is thebasal species of this genus.

Although we included only four specimens from Taiwan in ourtaxonomic study and DNA analysis, we accept the description of Taiwanese taxonof K. arbuscula var. acuminata (Takaki) Ochyra, which differs from that of theK. arbuscula in having longer and more sharply acuminate leaves, to be within amorphological variation of Pseudokindbergia. We conclude therefore thatK. arbuscula is absent in Taiwan, contrary to the treatment of Takaki (1956).

On the identity of Himalayan Pseudokindbergia dumosa and Chinese Bryhnia serricuspis

Pseudokindbergia dumosa is a rare species, treated earlier as an endemicto India and Nepal (Gangulee, 1978; Vohra, 1983). We studied four Himalayan


samples from India and Bhutan collected at different altitudinal belts (alt. 2400 to4100 m). Superficially, the four Himalayan specimens were quite similar to theEuropean K. praelonga in their growth form, leaf shape and dimensions, andlamina cells etc. However, neither specimen was shown to be K. praelonga (e.g. amember of Kindbergia I clade) in our molecular study, but deeply nested withinthe clade formed by the Chinese specimens. Hedenäs (2010) had suggestedalready that K. dumosa may be the correct species name for all Chinese specimenscalled “K. praelonga”. By studying the type materials of K. dumosa, we found thatthe species is morphologically quite similar also to Bryhnia serricuspis and allChinese specimens annotated in herbaria as “K. arbuscula” and “K. praelonga”.Their similarity includes the shape of proximal branch leaves, operculum andcapsule orientation (Figs 9-15). The new molecular analyses supported theirconspecific identity (Figs 22-24). Hypnum dumosum was published in 1859, thus,it has priority over Eurhynchium serricuspis (Müller, 1898) in nomenclaturalconsideration. The latter was lectotypified by Koponen (1987) and accepted byhim as a distinct taxon from K. praelonga. Based on a study of large collectionsof specimens, Ignatov et al. (2005) came to the conclusion that the characterdifferences seen between these two taxa showed a gradual transition across Chinain the leaf shape, so they had to be combined as one taxon. At about the sametime, Hu et al. (2008) accepted this species, but placed it in the genus Bryhnia, asB. serricuspis. Inferred from molecular data, Li et al. (2014) proposed theinclusion of the species recognized in Bryhnia (represented by B. novae-angliae,B. hultenii, and B. scabrida) in Brachythecium s.str., and further treated Bryhniaas a synonym of the latter. While B. serricuspis with Chinese and Himalayan“Kindbergia” species was nested within another independent clade (Kindbergia IIclade) (Figs 22-24). The distinction between B. serricuspis (actuallyPseudokindbergia) and other species of Bryhnia is not easy as their leaves aresimilar in appearance, however, plants of the former have more regular pinnatebranching, a more abrupt tapering acumen towards the leaf apex, and broader leafdecurrency (Ignatov et al., 2005).

Another opinion on Bryhnia serricuspis identity was its conspecificitywith Sciuro-hypnum reflexum (Qian, 1987), which was thought to occur insouthern China (Piippo, 1987). A later study of Hedenäs et al. (2012) found,however, that in that area occurs another speices, S. sichuanicum Ignatov etHedenäs, that have much in common in morphology with Pseudokindbargia,being a large plant, although without distinctively regular branching, and withmuch laxer basal areolation and an autoicous sexual condition (contrary todioicous condition in Pseudokindbergia).

Acknowledgements. Thanks are due to the curators and staff of BM, DUKE, FH,FI, MHA, MO, NICH, NY, PC, PE, S, SHNU, TNS and XJU, Dr. N. Nishimura and M.Lüth for loans of specimens, including types of several taxa. L. Hedenäs is thanked for hisvaluable reference. We are grateful to Dr. R. Ochyra and an anonymous reviewer for theirvaluable comments on the manuscript. This study was supported by the Natural ScienceFoundation of China (Grant No. 31270255, 31370237) and the Russian Foundation forBasic Researches (Grant No. 13-04-01592).

64 M. Li et al.

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APPENDIX

Details of voucher specimens and Genbank accession numbers used forITS, trnG, rpl16, trnL-F gene sequence analyses.

Subfamily: taxon, locality, collector, collectors number or herbariumnumber, herbarium acronym; Genbank accession numbers ITS (or ITS1/ITS2),trnG, rpl16, trnL-F; Dashes (–) indicate that no sequence was obtained, asterisks(*) indicate newly generated sequences.Brachythecioideae: Brachytheciastrum collinum (Schleich. ex Müll.Hal.) Ignatov et Huttunen,China, Xinjiang Prov., Qinghe Co., S. Mamtimin 15123 (XJU), KJ605684*, KJ605759*,KJ605719*, KJ605793*; Spain, Granada, Sierra Nevada, S.Rams et al., 28.VII.2004 (MUB),EU567475, EU567604, EU567538, –. Brachytheciastrum velutinum (Hedw.) Ignatov etHuttunen, Finland, Regio aboënsis, Karjalohja, M. Kiirikki s.n., 23.VIII.1988 (H), EU567476,EU567539, EU567605, –. Brachythecium buchananii (Hook.) A. Jaeger, China, Shaanxi Prov.,Y.F. Wang 166 (HSNU), KF434291, KF418126, KF418098, KF434264; China, Sichuan Prov.,Y.F. Wang et al. 102 (HSNU), KF434292, KF418127, KF418099, KF434265. Brachytheciumcirrosum (Schwägr.) Schimp., China, Hebei Prov., Mt. Xiaowutai, Q. Zuo 711 (HSNU),KF434293, KF418128, KF418100, KF434266. Brachythecium hultenii (E.B. Bartram) M. Li etY.F. Wang, China, Jilin Prov., Y.F. Wang 146 (HSNU), KF434278, KF418113, KF418085,KF434251. Brachythecium novae-angliae (Sull. et Lesq.) A. Jaeger, China, Shaanxi Prov.,Y.F. Wang 174 (HSNU), KF434283, KF418118, KF418090, KF434256; China, Taiwan Prov.,M. Li 203 (HSNU), KF434284, KF418119, KF418091, KF434257; Japan, Hokkaido,Kitahiroshima, Y.F. Wang 7240 (HSNU), KF434286, KF418121, KF418093, KF434259.Brachythecium rivulare Schimp., China, Shaanxi Prov., Y.F. Wang 311 (HSNU), KF434295,KF418130, KF418102, KF434268; South Korea, Cheju-do., S. He & J.S. Song 34633 (MO),KF434296, KF418131, KF418103, KF434269. Eurhynchiadelphus eustegia (Besch.) Ignatov etHuttunen, China, Jilin Prov., T. Koponen 36592 (H), -/AF403602, –, –, AF397790.Eurhynchiastrum pulchellum (Hedw.) Ignatov et Huttunen, Canada, British Columbia, Vitt35808a (MHA), GQ254298, –, –, –; Finland, Lohja, T. Koponen & S. Huttunen 1321 (H),FM161101, EF531024, EF530956, –. Frahmiella acicula (Broth.) Ignatov, Vanderpoorten etY.F. Wang, China, Shaanxi Prov., Wang 3566 (HSNU, MHA), GU075853, –, –, –; China, ShaanxiProv., Wang 4257 (HSNU, MHA), GU075852, –, –, –. Homalothecium lutescens (Hedw.)H. Rob., France, Cales, G. Een s.n., 9. June 1995 (S), EF617558, –, EF531051, –. Homalotheciumphilippeanum (Spruce) Schimp., China, Xinjiang Prov., S. Mamtimin 18706 (XJU), KJ605687*,KJ605762*, KJ605722*, KJ605796*. Kindbergia arbuscula (Broth.) Ochyra, Japan, Fukuoka-shiProv., Sawara-ku, Iiba, Nogouchi-valley, A. Fujita 65 (dupl. HSNU), KJ605717*, KJ605791*,KJ605757*, –; Japan, Nara-ken Prov., Yoshino-gun, Kawakami-mura, N. Nishimura 12819 (dupl.HSNU), -/ KJ605718*, KJ605792*, KJ605758*, KJ605831*. Kindbergia dumosa (Mitt.) Ignatov etHuttunen, Bhutan, Lhuntse Distr., G. & S. Miehe 00-441-25 (MHA), KJ659017*, KJ659023*,KJ659021*, KJ659027*; Bhutan, Wangdue Phodrang Distr. -1, G. & S. Miehe 00-420-18 (MHA),KJ659018*, KJ659024*, –, KJ659028*; Bhutan, Wangdue Phodrang Distr. -2, G. & S. Miehe 98-373-9 (MHA), KJ659019*, KJ659025*, –, KJ659029*; China, Gansu Prov., Z.T. Zhao & N.N. Yu589 (PE) (Bryhnia serricuspis), KJ605685*, KJ605760*, KJ605720*, KJ605794*; China, HunanProv.-1, T. Koponen et al. 53561 (H) (Bryhnia serricuspis), -/AF403590, –, –, –;. China, HunanProv.-2, T. Koponen et al. 50467 (H) (“K. praelonga”), DQ336907, –, –, –; China, Hunan Prov.,Zhangjiajie-1, T. Koponen et al. 52771 (MHA) (“K. praelonga”), KJ605701*, KJ605775*,KJ605736*, KJ605810*; China, Hunan Prov., Zhangjiajie-2, T. Koponen et al. 52381 (MHA) (“K.praelonga”), KJ605702*, KJ605776*, KJ605737*, KJ605811*; China, Shaanxi Prov.-1, Y.F. Wang374 (HSNU) (Bryhnia serricuspis), KJ605686*, KJ605761*, KJ605721*, KJ605795*; China,Shannxi Prov.-2, Y.F. Wang 37 (HSNU) (“K. arbuscula”), KJ605688*, –, KJ605723*, KJ605797*;China, Sichuan Prov., D.Z. Xie & J.S.Lou 172 (H) (“K. praelonga”), GQ849704, GQ849617, –, –;China, Sichuan Prov., Gonggashan-1, S.Q. Sun 231 (SHNU) (“K. arbuscula”), KJ605689*,KJ605763*, KJ605724*, KJ605798*; China, Sichuan Prov., Gonggashan-2, T. Cao & B.R. Zuo90592 (SHNU) (“K. arbuscula”), KJ605690*, KJ605764*, KJ605725*, KJ605799*; China, SichuanProv. Gonggashan-3, T. Cao & B.R. Zuo 90659 (SHNU) (“K. arbuscula”), KJ605691*,KJ605765*, KJ605726*, KJ605800*; China, Sichuan Prov., Heishan Co.-1, Y.F. Wang & M. Li sn-2 (HSNU) (“K. praelonga”), KJ605704*, KJ605778*, KJ605739*, KJ605813*; China, SichuanProv., Heishan Co.-2, Y.H. Wu s.n. (HSNU) (“K. praelonga”), KJ605703*, KJ605777*,

68 M. Li et al.

KJ605738*, KJ605812*; China, Sichuan Prov., Luding Co., Y. Jia 01821 (PE) (“K. praelonga”),KJ605692*, KJ605766*, KJ605727*, KJ605801*; China, Sichuan Prov., Tianquan Co., T. Cao &B.R., Zuo 91047 (SHNU) (“K. praelonga”), KJ605693*, KJ605767*, KJ605728*, KJ605802*;China, Sichuan Prov., Wenchuan Co., Y. Jia 06958 (PE) (“K. praelonga”), KJ605694*,KJ605768*, KJ605729*, KJ605803*; China, Taiwan Prov., Nantou Co.-1, S., He 36270 (MO) (“K.praelonga”), KJ605705*, KJ605779*, KJ605740*, KJ605814*; China, Taiwan Prov., Nantou Co.-2,Y.F. Wang & M. Li 202 (HSNU) (“K. arbuscula”), KJ605695*, KJ605769*, KJ605730*,KJ605804*; China, Yunnan Prov., Dali Co., Q. Liu & Q. Zuo 1290 (HSNU) (“K. arbuscula”),KJ605696*, KJ605770*, KJ605731*, KJ605805*; China, Yunnan Prov., Nujiang Co.,Gaoligongshan, Q. Liu & Q. Zuo 168 (HSNU) (“K. arbuscula”), KJ605697*, KJ605771*,KJ605732*, KJ605806*; India, Uttarakhand, M. Lüth 6643 (MHA), KJ659020*, KJ659026*,KJ659022*, KJ659030*. Kindbergia oregana (Sull.) Ochyra, USA, Idaho, Clearwater Co., K.L.Gray 3941 (MO), KJ605698*, KJ605772*, KJ605733*, KJ605807*; USA, Oregon, Clatsop Co.,C.E. & D.D. Darigo 3990 (MO), KJ605699*, KJ605773*, KJ605734*, KJ605808*; USA, Oregon,Hood River Co., B. Allen 28751 (MO), KJ605700*, KJ605774*, KJ605735*, KJ605809*.Kindbergia praelonga (Hedw.) Ochyra, Colombia, Dept. Cauca, S. Churchill et al. 17157 (H),GQ849707, GQ849620, –, –; Ecuador, Azuay Prov., W.R. Buck 39323 (S), KJ605706*, KJ605780*,KJ605741*, KJ605815*; Mexico, Estado de México, A. Cárdenas S. 2675 (H), GQ849696,GQ849608, –, –; Austria, Upper Austria, R. Krisai, B105472 (S), GQ849746, GQ849660,KJ605751*, KJ605825*; Australia, Victoria, H. Streimann 42657, B96040 (S), GQ849735,GQ849649, KJ605752*, KJ605826*; Azores, Sao Miguel, L. Hedenäs s.n., B42727 (S), GQ849677,GQ849589, KJ605753*, KJ605827*; England, Shropshire, L. Hedenäs s.n., B144669 (S),KJ605707*, KJ605781*, KJ605742*, KJ605816*; Germany, Badenwürttemberg, L. Hedenäs s.n.,B89252 (S), GQ849685, GQ849597, KJ605754*, KJ605828*; Madeira, Tibeira do Moreno,S. Fontinha 2 B22292 (S), GQ849687, GQ849599, KJ605755*, KJ605829*; Norway, Hordaland,L. Hedenäs s.n., B94298 (S), GQ849713, GQ849626, KJ605756*, KJ605830*; South Africa, CapeProv., S.L. Williams 1110. (H), GQ849697, GQ849609, –, –; Sweden, Södermanland, Utö.,L. Hedenäs s.n., B175998 (S), KJ605708*, KJ605782*, KJ605743*, KJ605817*; USA, Alaska,Sitak Co., N. Darigo 76 (MO), KJ605709*, KJ605783*, KJ605744*, KJ605818*; USA, Oregon,Hood River Co., B. Allen 28744 (MO), KJ605710*, KJ605784*, KJ605745*, KJ605819*; USA,Oregon, Linn Co., B. Goffinet 7990, B98287 (S), KJ605711*, KJ605785*, KJ605746*, –; USA,Washington, Clark Co., C.E. & D.D. Darigo 3982 (MO), KJ605712*, KJ605786*,–, KJ605820*;Western Carpathians, Pogorze Slaskie Foothills, S. Adam., B157666 (S), KJ605713*, KJ605787*,KJ605747*, KJ605821*. Myuroclada longiramea (Müll. Hal.) M. Li, Y.F. Wang, M.S.Ignatov etS.Huttunen, China, Hebei Prov., Y.F. Wang 19 (HSNU), KF434274, KF418109, KF418081,KF434247; Russia, Far East, Sakhalin, Tymovsk Distr., M.S. Ignatov 06-431 (MHA), KF434277,KF418112, KF418084, KF434250. Myuroclada maximoviczii (G.G. Borshch.) Steere etW.B. Schofield, China, Shaanxi Prov., Y.F. Wang 54 (HSNU), KF434299, KF418133, KF418106,KF434271. Sciuro-hypnum ornellanum (Molendo) Ignatov et Huttunen, China, Xinjiang Prov.,S. Mamtimin 15709 (XJU), KJ605714*, KJ605788*, KJ605748*, KJ605822*. Sciuro-hypnumreflexum (Starke) Ignatov et Huttunen, China, Sichuan Prov., Y.F. Wang & M. Li s.n. (HSNU),KF434300, KF418134, KF418107, KF434272. Scleropodium obtusifolium (Mitt.) Kindb., USA,CA, Mariposa Co., Yosemite Natl. PK., Shevock 31752 (UC), HM771748, –, HM772030, –.Scleropodium touretii (Brid.) L.F.Koch, USA, CA, Obispo Co., Klau Mine Rd., S.L. Carter 1288(UC), HM771722, –, HM772004, –. Unclejackia longisetula (E.B.Bartram) Ignatov, T.J.Kop. etD.H.Norris, Papua New Guinea, Morobe Prov., T. Koponen 32496 (H), -/AF395643, –, –,AF397794.

OUTGROUPSEurhynchioideae: Rhynchostegium pallenticaule Müll.Hal., China, Zhejiang Prov.,Y.F. Wang et al. 407 (HSNU), KJ605716*, KJ605790*, KJ605750*, KJ605824*.Helicodontoideae: Cirriphyllum piliferum (Hedw.) Grout, Finland, Regio aboënsis, Lohja,T. Koponen & S. Huttunen s.n., 24.V.1999 (H), EU567479, EU567608, EU567542, –.Oxyrrhynchium hians (Hedw.) Loeske, China, Zhejiang Prov., Y.F. Wang et al. 28 (HSNU),KF434301, KF418135, KF418108, KF434273.Meteoriaceae: Barbella flagellifera (Cardot) Nog., China, Zhejiang Prov. Y.F. Wang et al.1051 (HSNU), KJ672398*, KJ672405*, KJ672412*, –. Meteorium atrovariegatum Cardot etThér., China, Zhejiang Prov. Y.F. Wang et al. 679 (HSNU), KJ672399*, KJ672406*,KJ672413*, KJ672419*.

taxonomic re-assessment of kindbergia (brachytheciaceae ......the brachytheciaceae are a moss family...

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